Evidence from neuroimaging of grasping and tool use 35

In principle, human neuroimaging techniques like fMRI should provide a rather straightforward means for testing theories of divided parietal function for tool use versus grasping. In practice, however, the way is not so easy. First and foremost, the study of real actions with fMRI is inherently very challenging. In

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f ds motion is likely the number one cause of poor data quality; even very small movements of the head, especially if in time with the experimental paradigm, can lead to spurious activations and render results unreliable. Hand and arm movements can easily tran head motion, leading to signal artifacts that coincide with actions and contaminate responses of interest (i.e. neural driven responses tied to action performance). Also, even if the head is kept completely still during action performance, movements of the arm itself (indeed, any mass) in the magnetic field can also lead to MR signal perturbations (Barry et al., 2010). A second set of challenges relate to the limitations imposed by spa The bore size of typical MR units is very small (typically ~ 60 cm), limiting the range of arm and hand movements that can be performed; and in the case of tool use, space iss also put physical constraints on the size of tools that can be tested. Also, the subject configuration for most MR units is to lie supine in the scanner, making direct vision o real objects impossible without the use of mirrors. Even if subjects could tilt their hea so that viewing of objects and the manual workspace might be possible, standard whole- head radio frequency coils used in most MR setups do not easily allow for such tilted head configurations.

Fortunately, these technical hurdles can be overcome, and our lab has developed the strategies, resources, and equipment to do so. First, to solve issues of mass-

movement-related signal artifacts we use slow event-related methods such that potential signal perturbations due to arm/hand movements occur in real time, whereas neural-

related, blood oxygenation level dependent (BOLD) changes occur with a temporal lag. Thus, by spacing actions well apart in time, we can resolve neural-related signal chang from movement-related artifacts. Second, with specialized radio frequency coils and custom built stimulus presentation equipment we are able to scan participants in a head- tilted configuration to allow for direct viewing of objects while they perform real action es s. ethods, itm - ults of

spatial extents, or somatosensory feedback, or, in m

or real oject Finally, a combination of careful head ‘packing’, simple biofeedback m

recru ent of participants who are well informed and experienced with fMRI, and the use of small amplitude movements to limit transfer of arm motion to the head have proven successful in solving problems with action-induced head motion.

Unfortunately, challenges with comparisons of grasping and tool use with fMRI go beyond solving such technical hurdles. Case-in-point, consider an experiment aimed to test theories of divided parietal streams for grasping and tool use by comparing grasp to-move actions directly against grasp-to-use actions. While the predications of such an experiment are clear based on the patient work reviewed above, interpreting the res

such a subtraction is not without its problems. The two types of actions, grasping and tool use, differ so greatly in kinematics (e.g. complexity, duration, and extent), greater

activations for grasping-to-use may relate to such differences in general, rather than anything specific to tool use per se.

The problem stated above underscores a major weakness common to all tool use imaging studies to date. Of the few studies that have used real objects, tool use has been compared with conditions involving no object manipulation (i.e. pantomime tool use) (Hermsdorfer, Terlinden, Muhlau, Goldenberg, & Wohlschlager, 2007; Imazu, Sugio, Tanaka, & Inui, 2007), no overt action (i.e. imagined tool use) (Higuchi, Imamizu, & Kawato, 2007), or, quite specifically, the use of chopsticks to pick up objects versus grasping with the hand (Inoue et al., 2001). Thus, ‘tool use activations’ may relate to differences in motor complexities, durations,

any instances, all of the above. More common, studies do not involve object manipulation at all, but instead look at tool use pantomimed actions as a proxy f tool use (e.g. S. H. Choi et al., 2001; Johnson-Frey et al., 2005; Rumiati et al., 2004). Here again, control actions are not carefully equated for kinematic complexity. In Pr

3 (Chapter 4) of the current thesis, I present a novel tool use paradigm that solves this incessant problem of controlling for kinematic complexity. I use a visual priming paradigm to probe the neural substrates of learned tool use, while at the same time comparing trial types that involve the same tool use actions and thus the same motor outputs. My findings (and this new improved approach) serve to push the field forward, and provide a more selective account of the neural substrates of learned tool use

previously available.

In a recent review, Lewis (2006) performed a meta-analysis compiling the reports from 35 imaging studies across 64 distinct paradigms involving tools. The types of tasks

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main rtex, and posterior middle temporal cortex. Areas of the production network were bilaterally repr

Patterson, 2003). Conversely, ventral stream activations in tool use production tasks have nged from more perceptual/conceptual (answering questions, reading words, viewing pictures) to more motor-related (imagined tool use, pantomiming tool use), to actual tool manipulation (with real tools used; discussed above). Lewis distinguished between a conceptual versus production tool use network based on the number of paradigms showing activation overlap and the type of task used (conceptual versus production). The main areas of the conceptual network comprised left inferior frontal gyrus, left posterior middle temporal gyrus, and bilateral fusiform cortex, while the areas of the production network comprised PPC (both IPL and SPL), dorsal lateral premotor cortex, ventral premotor co

esented, but with clear left hemisphere prevalence in strength and extent of activity. While this separation is useful, the same data may also be taken quite differently. That is, with these same data one might instead highlight that activation patterns across a number studies show surprisingly high

proportions of overlap for both conceptual and action tasks. Indeed, as Scott Frey has emphasized in his reviews of the neuroimaging literature on tools, both dorsal and ventral stream areas are often activated for both motor and conceptual tasks (Frey, 2007;

Johnson-Frey, 2004). Dorsal stream activations for conceptual tasks have been taken as support for distributed accounts of conceptual knowledge stores (Barsalou, 2007). In this view, it is worth noting that several independent groups have shown that left IPL is activated more strongly during explicit retrieval of manipulation versus functional knowledge of tools (Boronat et al., 2005; Canessa et al., 2008; Kellenbach, Brett, &

been taken as support for the cooperative role of both dorsal and ventral streams underlying familiar tool use (Frey, 2007), in line with the basic model shown in Fi 1.3. However, this interpretation may be confounded. Defining contrasts often invo object versus non-object conditions, and thus ventral stream activity may be attributed visual object activity (or imagery). Also, most of these studies employ tool use

pantomime which may specifically recruit ventral stream resources independent of real tool use, as do other m

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emory-guided actions (Cohen, Cross, Tunik, Grafton, & Culham, 2009; Singh ents less ither ed role of n for sed a ined al, Kaufman, Valyear, & Culham, 2005) (however, see also Kroliczak, Cavina-Pratesi, Goodman, & Culham, 2007). In fact, pantomime in the absence of real 3D objects also obscures interpretation of parietal activations; added conceptual elem may ‘push around’ patterns of activity, giving rise to findings not otherwise

representative of real tool use. In summary, additional work is clearly needed to: i) verify the role of ventral stream areas in real tool use planning and implementation, and ii) identify potential differences between real and pantomime tool use.

Before concluding, a few additional imaging findings demand specific attention (despite some of the caveats just discussed). First, Johnson-Frey et al. (2005) showed that posterior parietal activity for tool use pantomime was strongly left-lateralized regard of which hand was used (see also Bohlhalter et al., 2009; Kroliczak & Frey, 2009). This contrasts with activation for grasping, which shows bilateral activations in AIP for e hand, although typically stronger activity in the hemisphere contralateral to the hand us for grasping (Begliomini, Nelini, Caria, Grodd, & Castiello, 2008; Culham et al., 2006; A. Stark & Zohary, 2008). The pattern is consistent with the proposed specialized the left lateral-IPL stream for learned tool use and its separation from the medial-SPL stream devoted to online control of more basic actions. With a clever “go”-“no-go” design, Johnson-Frey and colleagues (2005) were also able to tease apart activatio tool use pantomime planning versus execution. They showed a posterior-to-anterior continuum of planning-to-execution-related activity in inferior parietal cortex, remarkably consistent with the findings of another imaging study that independently surfaced at the same time (Fridman et al., 2006). Finally, Vingerhoets et al. (2009) u motor imagery task to compare the following conditions: imagined pointing-to, imag grasping-to-move, imagined grasping-to-use, and imagined grasping-and-using tools.

They also varied these conditions across familiar tools, unfamiliar tools, and simp shapes. In short, they report a collection of activation foci within the left IPS that are: i) more active for use versus move tasks, and/or ii) show sensitivity to tool familiarity. Again, these findings are consistent with the general idea that left inferior parietal cortex is specialized for learned tool use, and suggest that spatially distinct IPS populat

contribute to distinct aspects of tool use knowledge.